Evolutionary genetics and implications of small size and twinning in callitrichine primates

Abstract

New World monkeys (NWMs) are characterized by an extensive size range, with clawed NWMs (subfamily Callitrichinae, or callitrichines) such as the common marmoset manifesting diminutive size and unique reproductive adaptations. Perhaps the most notable of these adaptations is their propensity toward multiple gestations (i.e., dichorionic twins and trichorionic triplets). Indeed, with the exception of Goeldi's monkey (Callimico), callitrichine singleton pregnancies rarely occur. Multiple gestations seem to have coevolved with a suite of reproductive adaptations, including hematopoetic chimerism of siblings, suppression of reproduction in nondominant females, and cooperative alloparenting. The sequencing of the common marmoset (Callithrix jacchus) genome offers the opportunity to explore the genetic basis of these unusual traits within this primate lineage. In this study, we hypothesized that genetic changes arising during callitrichine evolution resulted in multiple ovulated ova with each cycle, and that these changes triggered adaptations that minimized complications common to multiple gestations in other primates, including humans. Callitrichine-specific nonsynonymous substitutions were identified in GDF9, BMP15, BMP4, and WFIKKN1. WFIKKN1, a multidomain protease inhibitor that binds growth factors and bone morphogenetic proteins, has nonsynonymous changes found exclusively in common marmosets and other tested callitrichine species that twin. In the one callitrichine species that does not produce twins (Callimico), this change has reverted back to the ancestral (nontwinning) primate sequence. Polymorphisms in GDF9 occur among human cohorts with a propensity for dizygotic twins, and polymorphisms in GDF9 and BMP15 are associated with twinning in sheep. We postulate that positive selection affected NWM growth patterns, with callitrichine miniaturization coevolving with a series of reproductive adaptations.reproductive biology | primate evolution

Possible asynchronous parturition in a multifetal strepsirrhine: Hapalemur meridionalis

“…It has been reported that twinning is common among H. alaotrensis, a close congener of H. meridionalis (Steyn and Feistner, 1994;Beattie and Feistner, 1998;Mutschler et al, 2000), and while it is less frequent among H. griseus (Haring and Davis, 1998), twinning is known to occur (Tan, 2000). Although lemurs are known for their high-frequency of multifetal pregnancies similar to some callitrichid primates (Bales et al, 2001;Harris et al, 2014), these also result in high infant mortality (Debyser, 1995;Parga and Lessnau, 2005;Volampeno et al, 2011). In some cases an accidental fall may cause or lead to death in a neonate (Morland, 1990), yet stillborn and infant mortality have been shown to increase with multifetal births, often with stress and infections linked to infant/juvenile mortality (Debyser, 1995).…”

“…Placentas do not necessarily need to be un-fused for this phenomenon to occur, as among humans a fused placenta from the first twin can remain in-utero until the birth of the second (de Jong et al, 1995). Dizygotic twinning is much more common than monozygotic twinning in humans (Hoekstra et al, 2008) and is known to occur in other non-human primates (Geissmann, 1990;Ely et al, 2006;Harris et al, 2014). Twinning rates among haplorrhine primates are low (e.g., Geissmann, 1990;Link et al, 2006;Huck et al, 2014;but see Bales et al, 2001 for an example of callitrichid twinning), however, it appears to be extremely common in primates with a bicornuate uterus, such as in Strepsirrhini, i.e., a suborder of Primates which includes lemurs, lorises, and galagos (Pasztor and van Horn, 1976;van Horn and Eaton, 1979;Benirschke and Miller, 1982;Parga and Lessnau, 2005;Tecot et al, 2013).…”

Coevolution of insulin-like growth factors, insulin and their receptors and binding proteins in New World Monkeys

“…Analysis of the marmoset genome [28,29] showed an acceleration in the rate of evolution of IGF1R and IGFBP2, and it was suggested that this was related to the reduced size seen in callitrichine NWM. The present study confirms this acceleration, but establishes that it largely stopped before divergence of Callithrix and Saimiri, i.e.…”

“…Recently the genomic sequence of a NWM, the marmoset (Callithrix jacchus) has been described in detail [28] providing evidence for rapid evolution of several proteins involved in growth regulation, including IGF1R and IGFBP2; this was linked to the reduction in size seen in the callitrichine NWM (marmosets and tamarins) [28,29]. Here sequences of the IGF1R, IR, IRRR and IGFBPs of primates and several non-primate outgroups have been derived from available databases, and examined in order to investigate further which of these proteins showed an episode of rapid evolution on the lineage leading to NWM, alongside the accelerated evolution noted previously for their cognate ligands [4].…”

WFIKKN1 and WFIKKN2: “Companion” proteins regulating TGFB activity

“…revealed differential expression of WFIKKN1 and WFIKKN2 in various tissues and conditions suggesting that their function is not limited to MSTN and GDF11 inhibition in muscle and skeletal tissues. Nevertheless, the role of members of this gene family in other tissues is still poorly understood despite evidence suggesting possible action in the inner ear [15], brain [16][17][18][19] and reproduction [20,21]. We summarize here current knowledge about WFIKKN1 and WFIKKN2 and propose a more generic function for these two proteins.…”